ORIGINAL ARTICLE

The origin of the inferior phrenic artery: a study in 32South Indian cadavers with a review of the literature

Origem da artéria frênica inferior: estudo em 32 cadáveres da Índiado Sul com revisão da literatura

Thejodhar Pulakunta1, Bhagath Kumar Potu1, Vasavi Rakesh Gorantla1, Muddanna S. Rao1,Sampath Madhyastha2, Venkata Ramana Vollala3

AbstractBackground: Considering the paucity of information presently

available concerning inferior phrenic arteries, a more definitive studyseemed appropriate and necessary, both for its potential clinicalapplications and to provide additional data to contemporaryanatomical literature.

Objective: Most anatomical textbooks of gross anatomy offer verylittle information concerning the anatomy and distribution of theinferior phrenic artery (IPA). For that reason, the origin of the IPAhas been studied and the available literature has been reviewed.

Methods: Thirty-two human adult cadavers preserved in formalinobtained from the departments of Anatomy, Kasturba MedicalCollege, Manipal and Mangalore were dissected and the origin of theIPA was studied.

Results: The IPA had its usual origin from the abdominal aorta in28 cases but in the remaining four cases, two were arising from theceliac trunk, one from the left gastric artery and one from the rightrenal artery.

Conclusion: The IPA usually originates from the aorta or celiacartery, and less frequently from the renal, hepatic or left gastric arteries.The IPA is a major source of collateral or parasitized arterial supplyto hepatocellular carcinoma, second only to the hepatic artery.Literature on the IPA origin and clinical implications of variation inits origin have been reviewed in this article.

Keywords: Inferior phrenic arteries, hepatocellular carcinoma,embolization, vascular variations.

ResumoContexto: Considerando a escassez de informações atualmente

disponíveis sobre artérias frênicas inferiores, um estudo mais definitivonos pareceu apropriado e necessário, tanto por suas potenciaisaplicações clínicas quanto para fornecer dados adicionais à literaturaanatômica contemporânea.

Objetivo: A maioria dos livros-texto de anatomia oferece muitopoucas informações referentes à anatomia e distribuição da artériafrênica inferior (AFI). Por este motivo, a origem da AFI foi investigadae a literatura disponível foi revisada.

Métodos: Trinta e dois cadáveres humanos adultos preservadosem formol e obtidos dos departamentos de anatomia do KasturbaMedical College, Manipal and Mangalore foram dissecados, e a origemda AFI foi investigada.

Resultados: A AFI teve sua origem habitual na aorta abdominalem 28 casos; no entanto, nos quatro casos restantes, duas originavam-sedo tronco celíaco, uma da artéria gástrica esquerda e uma da artériarenal direita.

Conclusão: A AFI geralmente origina-se da aorta ou artériacelíaca, e menos freqüentemente das artérias renal, hepática ou gástricaesquerda. A AFI é a maior fonte de fornecimento arterial colateral ouparasitado para carcinoma hepatocelular, ficando atrás somente daartéria hepática. A literatura sobre a origem da AFI e as implicaçõesclínicas de variação em sua origem foram revisadas neste artigo.

Palavras-chave: Artérias frênicas inferiores, carcinomahepatocelular, embolização, variações vasculares.

IntroductionAlthough descriptions of the right inferior phrenic

artery (RIPA) and left inferior phrenic artery (LIPA) aretypically very brief and lacking in detail in anatomy text-books, they have received increased attention in recentyears in the clinical literature. This stems largely fromthe discovery of the involvement of the right (most fre-quently) or left inferior phrenic arteries in the arterial

supply and growth of hepatocellular carcinoma(HCC).1,2 Indeed, the great importance of such knowl-edge lies in the fact that an unresectable HCC can betreated by transcatheter embolization of not only its typi-cal blood supply, the right or left hepatic arteries, butalso by embolization of a RIPA, if involved.1-4

Accordingly, with the appropriately targeted utiliza-tion of certain current cancer treatments hinging on a

1 . Department of Anatomy, Kasturba Medical College, Manipal, Karnataka, India.2 . Department of Anatomy, Kasturba Medical College, Mangalore, Karnataka, India.3 . Department of Anatomy, Melaka Manipal Medical College, Manipal, Karnataka, India.

Manuscript received May 21, 2007, accepted for publication Jun 08, 2007.

J Vasc Bras 2007;6(3):225-230.Copyright © 2007 by Sociedade Brasileira de Angiologia e de Cirurgia Vascular

225

thorough knowledge of the origin of the IPA, our cur-

rent study aimed at establishing this very fact. There are

few publications concerning the role and detailed

anatomy of the IPA with respect to their involvement in

HCC1,2,5 and, similarly, few have been produced with

direct focus on the elucidation of the origin and distri-

bution of these arteries.1,2,6 Quain, quoted by Pick &

Anson,7 was the first author to describe the origin of

the IPA. Tanabe et al.1 referred only to general textbook

descriptions of these arteries and Gokan et al.2 reported

on frequency of origin of the RIPA in a study of 16

patients. A study of 74 cadavers by Adachi8 is the larg-

est available concerning IPA. Modern anatomy text-

books offer few details of the anatomy of the inferior

phrenic arteries.9-11 Because transcatheter embolization

of HCC and other hepatic neoplasms often involves find-

ing the root of the RIPA, the interventional radiologist

or oncologist could potentially benefit from knowledge

of common variations in origin of these vessels and their

respective frequencies of occurrence. The importance of

the IPA is not limited to the treatment of HCC. Practi-

cally any hepatic neoplasm (including metastatic dis-

ease to the liver) may receive blood supply from the IPA.

In addition, there have been reports of gastric hemor-

rhage due to bleeding from the LIPA after treatment of

the left gastric artery with embolization.12

Vascular variations are constantly observed in dis-

section of adult cadavers.13 The inferior phrenic arter-

ies usually originate from the aorta or celiac artery, and

less frequently from the renal, hepatic or left gastric arter-

ies. The roentgenographic anatomy of the phrenic arter-

ies has been described in detail by Kahn et al.14 They

contribute to the arterial supply of the adrenal glands

and are thus important in angiographic examinations

for adrenal lesions.14,15

In general, these vessels, which supply the dia-

phragm, are of small caliber.13,16,17 The purpose of this

study was to analyze the origin of the inferior phrenic

arteries.

Methods

Thirty-two human adult cadavers preserved in for-

malin, obtained from the departments of anatomy, Kas-

turba Medical College, Manipal and Mangalore were

dissected and the origin of the inferior phrenic artery

was studied. The ages of the cadavers ranged between

28-56 years. To dissect the abdominal aorta, the pan-

creas was removed with the aid of scissors. All the gan-

glions and the nervous tissue around the arteries were

removed with the aid of a pincer and scissors to allow

observing the disposition of these inferior phrenic arter-

ies. After resection of tissues subjacent to the diaphrag-

matic crura and adherent tissues all along the median

arcuate ligament, these structures were exposed, allow-

ing observation of the origin of the IPA.

Results

The inferior phrenic artery showed a variant origin

in four out of 32 cases. It was seen to arise directly from

the celiac trunk in two cases (Figures 1 and 2) and there

was one case arising from the left gastric artery (Figure 3)

and another from the right renal artery (Figure 4). The

observations have been tabulated below in Table 1 and

Figure 5.

Table 1 - Gender, age, side and origin of the variant cases

Serial no Gender Age Side Origin

Case 1 Male 43 Left Celiac Trunk

Case 2 Female 29 Bilateral Celiac Trunk

Case 3 Male 35 Left Gastric Artery

Case 4 Female 54 Right Renal Artery*

* A coexisting supernumerary right renal artery from the aorta was also observed.

226 J Vasc Bras 2007, Vol. 6, Nº 3 The origin of the inferior phrenic artery – Pulakunta T et al.

Discussion

Considering the paucity of information presently

available concerning these arteries, a more definitive

study seemed appropriate and necessary, both for its

potential clinical applications and to provide additional

data to contemporary anatomical literature. In describ-

ing the origins of the IPA, the fourth edition of Mastery

of Surgery11 gives only brief mention of the aorta or

AA = abdominal aorta; ARRA = accessory right renal artery; IVC = inferiorvena cava; RIPA = right inferior phrenic artery; RK = right kidney; RRA =right renal artery; RSRG = right suprarenal gland.

Figure 4 - Right inferior phrenic artery arising from the rightrenal artery (case 4)

AA = abdominal aorta; CHA = common hepatic artery; CT = celiac trunk;LIPA = left inferior phrenic artery; SA = splenic artery.

Figure 1 - Left inferior phrenic artery arising from the celiactrunk (case 1). Splenic artery is reflected to the rightside, to show the origin of left inferior phrenicartery from celiac trunk

BD = bile duct; CA = cystic artery; CHA = common hepatic artery; CT = celiactrunk; GDA = gastroduodenal artery; LGA = left gastric artery; LHA = lefthepatic artery; LIPA = left inferior phrenic artery; RHA = right hepatic artery;RIPA = right inferior phrenic artery; RLL = right lobe of the liver; SA = splenicartery.

Figure 2 - Right and left inferior phrenic arteries arising fromthe celiac trunk (case 2)

CT = celiac trunk; LGA = left gastric artery; LIPA = left inferior phrenic artery;SA = splenic artery; SMA = superior mesenteric artery.

Figure 3 - Left inferior phrenic artery arising from the leftgastric artery (case 3)

The origin of the inferior phrenic artery – Pulakunta T et al. J Vasc Bras 2007, Vol. 6, Nº 3 227

celiac trunk, or the right renal artery as sources of the

IPA.

The English edition of Gray’s Anatomy10 gives a

slightly more complete account, claiming origins from

the aorta or celiac trunk, variably from common trunks,

and possibly from the renal artery. The American edi-

tion of Gray’s Anatomy9 gives the most complete text-

book account, claiming origins from both the celiac

trunk and aorta, as well as describing common trunk

origins and mentioning alternative origins, including the

renal or accessory renal arteries, the left gastric, hepatic,

and gonadal arteries. Interestingly, none of these refer-

ences provide statistical information regarding origin of

either the RIPA or LIPA.

In their analysis of the inferior phrenic arterialinvolvement in HCC, Tanabe et al.1 refer to otherauthors concerning the origins of the IPA, citing aorticand celiac trunk origins. The computed tomography(CT) study by Gokan et al.2 described these arteries withslightly greater detail and included actual percentages.They found that the most frequent origins were fromthe aorta and celiac trunk, with 46% of specimens pre-senting an aortic origin, most commonly on the rightside, and a celiac origin, most commonly on the left(52%). They also observed the RIPA arising from theright renal artery in 9% of cases studied. They men-tioned alternative origins as well (left gastric, hepatic,superior mesenteric, and spermatic), stating that suchorigins occurred with < 4% frequency on either the right

Case 1Case 1 Case 2Case 2

Case 3Case 3 Case 4Case 4

CT

CHA

AA

SA

LIPA

SMA

CHA

AA

SA

LIPA

LGA

LGA

CHA

SA

LIPA

SMA

AA

RIPA

AARK

RIPA

ARRA

ISRA

AA = abdominal aorta; ARRA = accessory right renal artery; CHA = common hepatic artery; CT = celiac trunk;ISRA = inferior suprarenal artery; LGA = left gastric artery; LIPA = left inferior phrenic artery; RIPA = rightinferior phrenic artery; RK = right kidney; SA = splenic artery; SMA = superior mesenteric artery.

Figure 5 - Schematic representations of the variations described above. Schema 1: originof left inferior phrenic artery from the celiac trunk; Schema 2: origin of bothinferior phrenic arteries from the celiac trunk; Schema 3: origin of left inferiorphrenic artery from the left gastric artery; Schema 4: origin of right inferiorphrenic artery from the right renal artery

228 J Vasc Bras 2007, Vol. 6, Nº 3 The origin of the inferior phrenic artery – Pulakunta T et al.

or left sides. Anatomical studies by Anson & McVay18

provided illustrations that depicted the IPA situated at

various levels vertically, but originating only from the

aorta or celiac trunk. No numerical data were provided

in their study. In an examination of 68 Japanese cadav-

ers, Piao et al.6 found the majority of the IPA arising

from the aorta (61.6%), with 28.2% of the IPA originat-

ing from the celiac trunk, and the remainder originating

from either renal, left gastric, or middle adrenal arter-

ies. Pick & Anson7 gave an impressive account of their

findings concerning various aspects of the inferior

phrenic arteries in their dissection of 200 cadavers.

Regarding origins, they found aortic and celiac sources

to be the most common (45.1 and 47.8%, respectively).

They claimed common trunks variably for both as well,

and even a common origin with the right internal sper-

matic artery. They found that < 7% arose variably from

the renal (5.8%), left gastric (2.3%), or hepatic arteries

(0.3%). This work is by far the most complete account

to date of the IPA origins.

However, in the current study the origin of the IPA

arteries from the celiac trunk was observed in two cases

(6.25%), one from the left gastric artery (3.125%) and

one from the right renal artery (3.125%) out of the 32

cadavers. In the remaining 28 cases it had its normal ori-

gin from the abdominal aorta. Loukas et al.19 reported

that, out of 300 cadavers they studied, the right IPA

originated from: a) celiac trunk in 40% of the speci-

mens; b) aorta in 38%; c) renal in 17%; d) left gastric in

3%; and e) hepatic artery proper in 2% of the speci-

mens. The left IPA originated from: a) celiac trunk in

47%; b) aorta in 45%; c) renal in 5%; d) left gastric in

2%; and e) hepatic artery proper in 1% of the speci-

mens. The current study showed similar findings, except

for the fact that the frequency of the IPA originating

from the celiac trunk was much lesser.

The IPA is a major source of collateral or parasit-

ized arterial supply to HCC, second only to the hepatic

artery.19 The right IPA was always associated with HCC

and served as the major collateral artery adjunct to the

hepatic artery. These findings could have major impli-

cations in the transcatheter embolization of HCC

patients. The knowledge of this type of variation shows

that surgeons must be cautious to avoid unintentional

sectioning of small-caliber arteries, as it may occur dur-

ing celiac artery decompression in compression syn-

drome of the celiac trunk by the median arcuate

ligament.

Presence of a supernumerary renal artery (as

observed in case 4) is due to the abnormal disappear-

ance or lack of formation of the lateral mesonephric

arteries and their connecting channels.20,21

We hope this study has provided valuable data to

researchers, clinicians and anatomists alike by enhanc-

ing the understanding of both the specific anatomy of

the inferior phrenic arteries and their potential signifi-

cance in supplying HCC and any number of other

tumors, primary or metastatic, to the liver, such as cho-

langiocarcinoma, hepatoblastoma and subcapsular

adenoma.22 For the clinician, in particular, treatments

such as transcatheter embolization of HCC call for

extensive knowledge of all possible variations of these

vessels, particularly their origins, and it is conceivable

that the application of this data will prove useful in the

discussion and treatment of other hepatic, suprarenal

or even diaphragmatic lesions unforeseen at the present

time.19

Acknowledgements

We would like to thank Dr. Narga Nair, Professor

and Head of the Department of Anatomy, KMC,

Manipal for her support. We would also like to thank

Mr. Nagaraj, Senior Artist, Center for Basic Sciences,

KMC, Manipal for his assistance with the illustrations.

A special thanks to Dr. Marios Loukas, MD, PhD,

Department of Anatomy, American University of the

Caribbean, Jordan Road, Cupecoy, Lowlands, Saint

Maarten, Netherlands Antilles for his help.

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Correspondence:Bhagath Kumar.PotuDepartment of Anatomy, Center for Basic SciencesKasturba Medical College576104Manipal, Karnataka – IndiaTel.: + 91 820 2922327E-mail: potu_kumar2000@yahoo.co.in

230 J Vasc Bras 2007, Vol. 6, Nº 3 The origin of the inferior phrenic artery – Pulakunta T et al.